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Destabilization of the Bacterial Interactome Identifies Nutrient Restriction-Induced Dysbiosis in Insect Guts

Marasco, Ramona; Fusi, Marco; Callegari, Matteo; Jucker, Costanza; Mapelli, Francesca; Borin, Sara; Savoldelli, Sara; Daffonchio, Daniele; Crotti, Elena

Authors

Ramona Marasco

Marco Fusi

Matteo Callegari

Costanza Jucker

Francesca Mapelli

Sara Borin

Sara Savoldelli

Daniele Daffonchio

Elena Crotti



Abstract

Stress-associated dysbiosis of microbiome can have several configurations that, under an energy landscape conceptual framework, can change from one configuration to another due to different alternating selective forces. It has been proposed—according to the Anna Karenina Principle—that in stressed individuals the microbiome are more dispersed (i.e., with a higher within-beta diversity), evidencing the grade of dispersion as indicator of microbiome dysbiosis. We hypothesize that although dysbiosis leads to different microbial communities in terms of beta diversity, these are not necessarily differently dispersed (within-beta diversity), but they form disrupted networks that make them less resilient to stress. To test our hypothesis, we select nutrient restriction (NR) stress that impairs host fitness but does not introduce overt microbiome selectors, such as toxic compounds and pathogens. We fed the polyphagous black soldier fly, Hermetia illucens, with two NR diets and a control full-nutrient (FN) diet. NR diets were dysbiotic because they strongly affected insect growth and development, inducing significant microscale changes in physiochemical conditions of the gut compartments. NR diets established new configurations of the gut microbiome compared to FN-fed guts but with similar dispersion. However, these new configurations driven by the deterministic changes induced by NR diets were reflected in rarefied, less structured, and less connected bacterial interactomes. These results suggested that while the dispersion cannot be considered a consistent indicator of the unhealthy state of dysbiotic microbiomes, the capacity of the community members to maintain network connections and stability can be an indicator of the microbial dysbiotic conditions and their incapacity to sustain the holobiont resilience and host homeostasis.

Journal Article Type Article
Acceptance Date Nov 30, 2021
Online Publication Date Jan 5, 2022
Publication Date 2022-02
Deposit Date Feb 1, 2022
Publicly Available Date Feb 1, 2022
Journal Microbiology Spectrum
Print ISSN 2165-0497
Publisher American Society for Microbiology
Peer Reviewed Peer Reviewed
Volume 10
Issue 1
DOI https://doi.org/10.1128/spectrum.01580-21
Keywords nutrient restriction, dysbiosis, bacterial microbiome, beta-diversity, dispersion, black soldierfly, interactome, co-occurrence network, gut, keystone species
Public URL http://researchrepository.napier.ac.uk/Output/2839636

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